Dietary supplementation of thiamine enhances colonic integrity and modulates mucosal inflammation injury in goats challenged by lipopolysaccharide and low pH

Abstract The current study aimed to investigate the protective effects of dietary thiamine supplementation on the regulation of colonic integrity and mucosal inflammation in goats fed a high-concentrate (HC) diet. Twenty-four Boer goats (live weight of 35·62 (sem 2·4) kg) were allocated to three groups (CON: concentrate/forage = 30:70; HC; concentrate/forage = 70:30 and HCT: concentrate/forage = 70:30 with 200 mg thiamine/kg DMI) for 12 weeks. Results showed that compared with the HC treatment, the HCT group had a significantly higher ruminal pH value from 0 to 12 h after the feeding. The haematoxylin–eosin staining showed that desquamation and severe cellular damage were observed in the colon epithelium of the HC group, whereas the HCT group exhibited more structural integrity of the epithelial cell morphology. Compared with the HC treatment, the HCT group showed a markedly increase in pyruvate dehydrogenase and α-ketoglutarate dehydrogenase enzymes activity. The mRNA expressions in the colonic epithelium of SLC19A2, SLC19A3, SLC25A19, Bcl-2, occludin, claudin-1, claudin-4 and ZO-1 in the HCT group were significantly increased in comparison with the HC diet treatment. Compared with the HC treatment, the HCT diet significantly increased the protein expression of claudin-1 and significantly decreased the protein expression of NF-κB-related proteins p65. The results show that dietary thiamine supplementation could improve the colon epithelial barrier function and alleviate mucosal inflammation injury in goats after lipopolysaccharide and low pH challenge.

[1]  Brow,et al.  Newcastle upon Tyne , 2021, A Life in Balkan Archaeology.

[2]  Y. Ma,et al.  Thiamine ameliorates metabolic disorders induced by a long-term high-concentrate diet and promotes rumen epithelial development in goats. , 2021, Journal of dairy science.

[3]  Hao Zhang,et al.  Thiamine Alleviates High-Concentrate-Diet-Induced Oxidative Stress, Apoptosis, and Protects the Rumen Epithelial Barrier Function in Goats , 2021, Frontiers in Veterinary Science.

[4]  Junhu Yao,et al.  Illumina Sequencing and Metabolomics Analysis Reveal Thiamine Modulation of Ruminal Microbiota and Metabolome Characteristics in Goats Fed a High-Concentrate Diet , 2021, Frontiers in Microbiology.

[5]  Y. Lei,et al.  Supranutritional selenium level minimizes high concentrate diet-induced epithelial injury by alleviating oxidative stress and apoptosis in colon of goat , 2020, BMC Veterinary Research.

[6]  P. Griebel,et al.  Effects of lipopolysaccharide exposure in primary bovine ruminal epithelial cells. , 2020, Journal of dairy science.

[7]  J. Osorio,et al.  Thiamine ameliorates inflammation of the ruminal epithelium of Saanen goats suffering from subacute ruminal acidosis. , 2019, Journal of dairy science.

[8]  H. Dai,et al.  Sodium Butyrate Modulates Mucosal Inflammation Injury Mediated by GPR41/43 in the Cecum of Goats Fed a High Concentration Diet , 2019, Front. Physiol..

[9]  Q. Zebeli,et al.  Diet-induced inflammation: From gut to metabolic organs and the consequences for the health and longevity of ruminants. , 2018, Research in veterinary science.

[10]  Lipeng Gao,et al.  Sodium Butyrate Improves High-Concentrate-Diet-Induced Impairment of Ruminal Epithelium Barrier Function in Goats. , 2018, Journal of agricultural and food chemistry.

[11]  X. Nan,et al.  Thiamine status, metabolism and application in dairy cows: a review , 2018, British Journal of Nutrition.

[12]  Y. Beckers,et al.  Illumina Sequencing Approach to Characterize Thiamine Metabolism Related Bacteria and the Impacts of Thiamine Supplementation on Ruminal Microbiota in Dairy Cows Fed High-Grain Diets , 2017, Front. Microbiol..

[13]  Y. Beckers,et al.  Thiamine supplementation facilitates thiamine transporter expression in the rumen epithelium and attenuates high-grain-induced inflammation in low-yielding dairy cows. , 2017, Journal of dairy science.

[14]  Weiyun Zhu,et al.  In vitro effects of sodium bicarbonate buffer on rumen fermentation, levels of lipopolysaccharide and biogenic amine, and composition of rumen microbiota. , 2017, Journal of the science of food and agriculture.

[15]  P. Møller,et al.  Gut microbiota‐derived lipopolysaccharide uptake and trafficking to adipose tissue: implications for inflammation and obesity , 2016, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[16]  M. Wagner,et al.  Epimural Indicator Phylotypes of Transiently-Induced Subacute Ruminal Acidosis in Dairy Cattle , 2016, Front. Microbiol..

[17]  Dirk Roos,et al.  Neutrophils: Between Host Defence, Immune Modulation, and Tissue Injury , 2015, PLoS pathogens.

[18]  B. Ju,et al.  Ghrelin inhibits BSCB disruption/hemorrhage by attenuating MMP-9 and SUR1/TrpM4 expression and activation after spinal cord injury. , 2014, Biochimica et biophysica acta.

[19]  R. Zhao,et al.  High Concentrate Diet Induced Mucosal Injuries by Enhancing Epithelial Apoptosis and Inflammatory Response in the Hindgut of Goats , 2014, PloS one.

[20]  R. Zhao,et al.  A high-concentrate diet induced colonic epithelial barrier disruption is associated with the activating of cell apoptosis in lactating goats , 2014, BMC Veterinary Research.

[21]  Dian Gao,et al.  Molecular cloning, immunohistochemical localization, characterization and expression analysis of caspase-9 from the purse red common carp (Cyprinus carpio) exposed to cadmium. , 2013, Aquatic toxicology.

[22]  N. Shaheen,et al.  Gastroesophageal reflux activates the NF-κB pathway and impairs esophageal barrier function in mice. , 2013, American journal of physiology. Gastrointestinal and liver physiology.

[23]  I. Goldman,et al.  Folate and thiamine transporters mediated by facilitative carriers (SLC19A1-3 and SLC46A1) and folate receptors. , 2013, Molecular aspects of medicine.

[24]  Qiurong Li,et al.  Lipopolysaccharide-Induced Bacterial Translocation Is Intestine Site-Specific and Associates with Intestinal Mucosal Inflammation , 2012, Inflammation.

[25]  D. Green,et al.  Mitochondrial pathway of apoptosis is ancestral in metazoans , 2012, Proceedings of the National Academy of Sciences.

[26]  E. Khafipour,et al.  Subacute ruminal acidosis (SARA), endotoxins and health consequences , 2012 .

[27]  R. Curi,et al.  Regulation of Inflammation by Short Chain Fatty Acids , 2011, Nutrients.

[28]  L. Armentano,et al.  Ruminant Nutrition Symposium: Productivity, digestion, and health responses to hindgut acidosis in ruminants. , 2011, Journal of animal science.

[29]  D. Ye,et al.  Occludin regulates macromolecule flux across the intestinal epithelial tight junction barrier. , 2011, American journal of physiology. Gastrointestinal and liver physiology.

[30]  G. Schmid-Schönbein,et al.  Nuclear Factor Kappa B and Matrix Metalloproteinase Induced Receptor Cleavage in the Spontaneously Hypertensive Rat , 2011, Hypertension.

[31]  C. Ricordi,et al.  Endotoxin Deactivation by Transient Acidification , 2010, Cell transplantation.

[32]  M. Fear,et al.  Thiamine supplementation increases serum thiamine and reduces pyruvate and lactate levels in burn patients. , 2010, Burns : journal of the International Society for Burn Injuries.

[33]  M. Balda,et al.  Dynamics and functions of tight junctions. , 2010, Trends in cell biology.

[34]  E. Khafipour,et al.  A grain-based subacute ruminal acidosis challenge causes translocation of lipopolysaccharide and triggers inflammation. , 2009, Journal of dairy science.

[35]  M. Gareau,et al.  Pathophysiological mechanisms of stress-induced intestinal damage. , 2008, Current molecular medicine.

[36]  B. McBride,et al.  Subacute ruminal acidosis in dairy cows: the physiological causes, incidence and consequences. , 2008, Veterinary journal.

[37]  G. Jan,et al.  Acidic extracellular pH shifts colorectal cancer cell death from apoptosis to necrosis upon exposure to propionate and acetate, major end-products of the human probiotic propionibacteria , 2007, Apoptosis.

[38]  A. D. Kennedy,et al.  Subacute ruminal acidosis induces ruminal lipopolysaccharide endotoxin release and triggers an inflammatory response. , 2005, Journal of dairy science.

[39]  G. Gibson,et al.  Tricarboxylic acid cycle enzymes following thiamine deficiency , 2004, Neurochemistry International.

[40]  L. Bertók.  Bile acids in physico-chemical host defence. , 2004, Pathophysiology : the official journal of the International Society for Pathophysiology.

[41]  D. Green,et al.  Role of Bcl-2 family members in immunity and disease. , 2004, Biochimica et biophysica acta.

[42]  M. Dabak,et al.  Thiamine deficiency in sheep with chronic rumen acidosis , 2004, Veterinary Record.

[43]  I. Goldman,et al.  SLC19A3 encodes a second thiamine transporter ThTr2. , 2001, Biochimica et biophysica acta.

[44]  C. Beglinger,et al.  Effect of ischemia on intestinal permeability of lipopolysaccharides , 2001, European journal of clinical investigation.

[45]  N. Mackman,et al.  LPS induction of gene expression in human monocytes. , 2001, Cellular signalling.

[46]  P. Zammit,et al.  Comparison of cattle and sheep colonic permeabilities to horseradish peroxidase and hamster scrapie prion protein in vitro , 1999, Gut.

[47]  G. Khorasani,et al.  Influence of carbohydrate source and buffer on rumen fermentation characteristics, milk yield, and milk composition in early-lactation Holstein cows. , 1999, Journal of dairy science.

[48]  James M. Anderson,et al.  The Tight Junction Protein ZO-1 Establishes a Link between the Transmembrane Protein Occludin and the Actin Cytoskeleton* , 1998, The Journal of Biological Chemistry.

[49]  Keisuke Kuida,et al.  Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice , 1996, Nature.

[50]  P. Andersen,et al.  Endotoxin and Arachidonic Acid Metabolites in Portal, Hepatic and Arterial Blood of Cattle with Acute Ruminai Acidosis , 1994, Acta Veterinaria Scandinavica.

[51]  H. Martens,et al.  The effect of low mucosal pH on sodium and chloride movement across the isolated rumen mucosa of sheep. , 1989, Quarterly journal of experimental physiology.

[52]  R. Ulevitch,et al.  A family of lipopolysaccharide binding proteins involved in responses to gram-negative sepsis. , 1988, The Journal of biological chemistry.

[53]  J. Cohen,et al.  The relationship between faecal endotoxin and faecal microflora of the C57BL mouse , 1985, Journal of Hygiene.

[54]  S. Schenker,et al.  Thiamine transport in thiamine-deficient rats. Role of the unstirred water layer. , 1976, Biochimica et biophysica acta.

[55]  R. G. Gunn,et al.  Subjective assessment of body fat in live sheep , 1969, The Journal of Agricultural Science.

[56]  M. P. Bryant,et al.  Some Nutritional Requirements of the Genus Ruminococcus. , 1961, Applied microbiology.

[57]  N. Gabler,et al.  Endotoxin, inflammation, and intestinal function in livestock , 2017 .

[58]  E. Khafipour,et al.  Effects of subacute ruminal acidosis challenges on fermentation and endotoxins in the rumen and hindgut of dairy cows. , 2012, Journal of dairy science.

[59]  J. O’Kusky,et al.  Saccharomyces boulardii ameliorates Citrobacter rodentium-induced colitis through actions on bacterial virulence factors. , 2008, American journal of physiology. Gastrointestinal and liver physiology.

[60]  R. Shaver,et al.  Dietary forage and nonfiber carbohydrate contents influence B-vitamin intake, duodenal flow, and apparent ruminal synthesis in lactating dairy cows. , 2006, Journal of dairy science.

[61]  Thomas D. Schmittgen,et al.  Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2 2 DD C T Method , 2022 .